Differential distribution of peroxisomal proteins points to specific roles of peroxisomes in the murine retina.
Metabolism
PUFA
Plasmalogens
Retina
Retinal pigment epithelium
Zellweger syndrome
β-Oxidation
Journal
Molecular and cellular biochemistry
ISSN: 1573-4919
Titre abrégé: Mol Cell Biochem
Pays: Netherlands
ID NLM: 0364456
Informations de publication
Date de publication:
Jun 2019
Jun 2019
Historique:
received:
25
06
2018
accepted:
14
12
2018
pubmed:
4
1
2019
medline:
18
5
2019
entrez:
4
1
2019
Statut:
ppublish
Résumé
The retinal pathology in peroxisomal disorders suggests that peroxisomes are important to maintain retinal homeostasis and function. These ubiquitous cell organelles are mainly involved in lipid metabolism, which comprises α- and β-oxidation and ether lipid synthesis. Although peroxisomes were extensively studied in liver, their role in the retina still remains to be elucidated. As a first step in gaining more insight into the role of peroxisomes in retinal physiology, we performed immunohistochemical stainings, immunoblotting and enzyme activity measurements to reveal the distribution of peroxisomes and peroxisomal lipid metabolizing enzymes in the murine retina. Whereas peroxisomes were detected in every retinal layer, we found a clear differential distribution of the peroxisomal lipid metabolizing enzymes in the neural retina compared to the retinal pigment epithelium. In particular, the ABC transporters that transfer lipid substrates into the organelle as well as several enzymes of the β-oxidation pathway were enriched either in the neural retina or in the retinal pigment epithelium. In conclusion, our results strongly indicate that peroxisome function varies between different regions in the murine retina.
Identifiants
pubmed: 30604065
doi: 10.1007/s11010-018-3489-3
pii: 10.1007/s11010-018-3489-3
doi:
Substances chimiques
ATP-Binding Cassette Transporters
0
Eye Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
53-62Subventions
Organisme : KU Leuven
ID : C14/18/088
Organisme : Hercules type 3
ID : ZW09-03
Références
Islinger M, Cardoso MJ, Schrader M (2010) Be different–the diversity of peroxisomes in the animal kingdom. Biochim Biophys Acta 1803:881–897. https://doi.org/10.1016/j.bbamcr.2010.03.013
doi: 10.1016/j.bbamcr.2010.03.013
pubmed: 20347886
Van Veldhoven PP (2010) Biochemistry and genetics of inherited disorders of peroxisomal fatty acid metabolism. J Lipid Res 51:2863–2895. https://doi.org/10.1194/jlr.R005959
doi: 10.1194/jlr.R005959
pubmed: 20558530
pmcid: 2936746
Wanders RJ, Waterham HR (2006) Biochemistry of mammalian peroxisomes revisited. Annu Rev Biochem 75:295–332. https://doi.org/10.1146/annurev.biochem.74.082803.133329
doi: 10.1146/annurev.biochem.74.082803.133329
pubmed: 16756494
Hoon M, Okawa H, Della Santina L, Wong RO (2014) Functional architecture of the retina: development and disease. Prog Retin Eye Res 42:44–84. https://doi.org/10.1016/j.preteyeres.2014.06.003
doi: 10.1016/j.preteyeres.2014.06.003
pubmed: 24984227
pmcid: 4134977
Strauss O (2005) The retinal pigment epithelium in visual function. Physiol Rev 85:845–881. https://doi.org/10.1152/physrev.00021.2004
doi: 10.1152/physrev.00021.2004
pubmed: 15987797
Robison WG Jr, Kuwabara T (1975) Microperoxisomes in retinal pigment epithelium. Invest Ophthalmol 14:866–872
pubmed: 810456
Leuenberger PM, Novikoff AB (1975) Studies on microperoxisomes. VII. Pigment epithelial cells and other cell types in the retina of rodents. J Cell Biol 65:324–334
doi: 10.1083/jcb.65.2.324
pubmed: 1168648
Beard ME, Davies T, Holloway M, Holtzman E (1988) Peroxisomes in pigment epithelium and Muller cells of amphibian retina possess D-amino acid oxidase as well as catalase. Exp Eye Res 47:795–806
doi: 10.1016/0014-4835(88)90063-2
pubmed: 2905671
Deguchi J, Yamamoto A, Fujiki Y, Uyama M, Tsukahara I, Tashiro Y (1992) Localization of nonspecific lipid transfer protein (nsLTP = sterol carrier protein 2) and acyl-CoA oxidase in peroxisomes of pigment epithelial cells of rat retina. J Histochem Cytochem 40:403–410. https://doi.org/10.1177/40.3.1552178
doi: 10.1177/40.3.1552178
pubmed: 1552178
Hazlett LD, Hazlett JC, Ireland M, Bradley RH (1978) Microperoxisomes in retinal epithelium and tapetum lucidum of the American opossum. Exp Eye Res 27:343–348
doi: 10.1016/0014-4835(78)90168-9
pubmed: 710543
Atalla L, Fernandez MA, Rao NA (1987) Immunohistochemical localization of catalase in ocular tissue. Curr Eye Res 6:1181–1187
doi: 10.3109/02713688709025227
pubmed: 3500016
St Jules R, Kennard J, Setlik W, Holtzman E (1992) Frog cones as well as Muller cells have peroxisomes. Exp Eye Res 54:1–8
doi: 10.1016/0014-4835(92)90062-W
pubmed: 1347269
Schad A, Fahimi HD, Volkl A, Baumgart E (2003) Expression of catalase mRNA and protein in adult rat brain: detection by nonradioactive in situ hybridization with signal amplification by catalyzed reporter deposition (ISH-CARD) and immunohistochemistry (IHC)/immunofluorescence (IF). J Histochem Cytochem 51:751–760. https://doi.org/10.1177/002215540305100606
doi: 10.1177/002215540305100606
pubmed: 12754286
Lenzen S, Drinkgern J, Tiedge M (1996) Low antioxidant enzyme gene expression in pancreatic islets compared with various other mouse tissues. Free Radic Biol Med 20:463–466
doi: 10.1016/0891-5849(96)02051-5
pubmed: 8720919
Grant P, Ahlemeyer B, Karnati S, Berg T, Stelzig I, Nenicu A, Kuchelmeister K, Crane DI, Baumgart-Vogt E (2013) The biogenesis protein PEX14 is an optimal marker for the identification and localization of peroxisomes in different cell types, tissues, and species in morphological studies. Histochem Cell Biol 140:423–442. https://doi.org/10.1007/s00418-013-1133-6
doi: 10.1007/s00418-013-1133-6
pubmed: 23959168
Zaki MS, Heller R, Thoenes M, Nurnberg G, Stern-Schneider G, Nurnberg P, Karnati S, Swan D, Fateen E, Nagel-Wolfrum K, Mostafa MI, Thiele H, Wolfrum U, Baumgart-Vogt E, Bolz HJ (2016) PEX6 is expressed in photoreceptor cilia and mutated in deafblindness with enamel dysplasia and microcephaly. Hum Mutat 37:170–174. https://doi.org/10.1002/humu.22934
doi: 10.1002/humu.22934
pubmed: 26593283
Smith CE, Poulter JA, Levin AV, Capasso JE, Price S, Ben-Yosef T, Sharony R, Newman WG, Shore RC, Brookes SJ, Mighell AJ, Inglehearn CF (2016) Spectrum of PEX1 and PEX6 variants in Heimler syndrome. Eur J Hum Genet 24:1565–1571. https://doi.org/10.1038/ejhg.2016.62
doi: 10.1038/ejhg.2016.62
pubmed: 27302843
pmcid: 5026821
Braverman NE, D’Agostino MD, Maclean GE (2013) Peroxisome biogenesis disorders: biological, clinical and pathophysiological perspectives. Dev Disabil Res Rev 17:187–196. https://doi.org/10.1002/ddrr.1113
doi: 10.1002/ddrr.1113
pubmed: 23798008
Ruether K, Baldwin E, Casteels M, Feher MD, Horn M, Kuranoff S, Leroy BP, Wanders RJ, Wierzbicki AS (2010) Adult Refsum disease: a form of tapetoretinal dystrophy accessible to therapy. Surv Ophthalmol 55:531–538. https://doi.org/10.1016/j.survophthal.2010.03.007
doi: 10.1016/j.survophthal.2010.03.007
pubmed: 20850855
Grainger BT, Papchenko TL, Danesh-Meyer HV (2010) Optic nerve atrophy in adrenoleukodystrophy detectable by optic coherence tomography. J Clin Neurosci 17:122–124. https://doi.org/10.1016/j.jocn.2009.08.019
doi: 10.1016/j.jocn.2009.08.019
pubmed: 20004581
Abe Y, Honsho M, Nakanishi H, Taguchi R, Fujiki Y (2014) Very-long-chain polyunsaturated fatty acids accumulate in phosphatidylcholine of fibroblasts from patients with Zellweger syndrome and acyl-CoA oxidase1 deficiency. Biochim Biophys Acta 1841:610–619. https://doi.org/10.1016/j.bbalip.2014.01.001
doi: 10.1016/j.bbalip.2014.01.001
pubmed: 24418004
Ferdinandusse S, Denis S, Mooijer PA, Zhang Z, Reddy JK, Spector AA, Wanders RJ (2001) Identification of the peroxisomal beta-oxidation enzymes involved in the biosynthesis of docosahexaenoic acid. J Lipid Res 42:1987–1995
pubmed: 11734571
Martinez M (2001) Restoring the DHA levels in the brains of Zellweger patients. J Mol Neurosci 16:309 – 16; discussion 317 – 21. https://doi.org/10.1385/jmn:16:2-3:309
Troffer-Charlier N, Doerflinger N, Metzger E, Fouquet F, Mandel JL, Aubourg P (1998) Mirror expression of adrenoleukodystrophy and adrenoleukodystrophy related genes in mouse tissues and human cell lines. Eur J Cell Biol 75:254–264. https://doi.org/10.1016/s0171-9335(98)80121-0
doi: 10.1016/S0171-9335(98)80121-0
pubmed: 9587057
Burgoyne T, Lane A, Laughlin WE, Cheetham ME, Futter CE (2018) Correlative light and immuno-electron microscopy of retinal tissue cryostat sections. PLoS One 13:e0191048. https://doi.org/10.1371/journal.pone.0191048
doi: 10.1371/journal.pone.0191048
pubmed: 29315318
pmcid: 5760081
Miceli MV, Liles MR, Newsome DA (1994) Evaluation of oxidative processes in human pigment epithelial cells associated with retinal outer segment phagocytosis. Exp Cell Res 214:242–249. https://doi.org/10.1006/excr.1994.1254
doi: 10.1006/excr.1994.1254
pubmed: 8082727
Ng MC, Shichi H (1989) Peroxisomal palmityl CoA oxidase activity in ocular tissues and cultured ciliary epithelial cells. J Ocul Pharmacol 5:65–70
doi: 10.1089/jop.1989.5.65
pubmed: 2715677
Kobayashi K, Kobayashi H, Ueda M, Honda Y (1997) Expression of 17 beta-hydroxysteroid dehydrogenase type IV in chick retinal pigment epithelium. Exp Eye Res 64:719–726. https://doi.org/10.1006/exer.1996.0262
doi: 10.1006/exer.1996.0262
pubmed: 9245902
Acar N, Gregoire S, Andre A, Juaneda P, Joffre C, Bron AM, Creuzot-Garcher CP, Bretillon L (2007) Plasmalogens in the retina: in situ hybridization of dihydroxyacetone phosphate acyltransferase (DHAP-AT)--the first enzyme involved in their biosynthesis–and comparative study of retinal and retinal pigment epithelial lipid composition. Exp Eye Res 84:143–151. https://doi.org/10.1016/j.exer.2006.09.009
doi: 10.1016/j.exer.2006.09.009
pubmed: 17081518
Baes M, Huyghe S, Carmeliet P, Declercq PE, Collen D, Mannaerts GP, Van Veldhoven PP (2000) Inactivation of the peroxisomal multifunctional protein-2 in mice impedes the degradation of not only 2-methyl-branched fatty acids and bile acid intermediates but also of very long chain fatty acids. J Biol Chem 275:16329–16336. https://doi.org/10.1074/jbc.M001994200
doi: 10.1074/jbc.M001994200
pubmed: 10748062
Kawaguchi K, Morita M (2016) ABC transporter subfamily D: distinct differences in behavior between ABCD1-3 and ABCD4 in subcellular localization, function, and human disease. Biomed Res Int 2016:6786245. https://doi.org/10.1155/2016/6786245
doi: 10.1155/2016/6786245
pubmed: 27766264
pmcid: 5059523
Yagita Y, Shinohara K, Abe Y, Nakagawa K, Al-Owain M, Alkuraya FS, Fujiki Y (2017) Deficiency of a retinal dystrophy protein, acyl-CoA binding domain-containing 5 (ACBD5), impairs peroxisomal beta-oxidation of very-long-chain fatty acids. J Biol Chem 292:691–705. https://doi.org/10.1074/jbc.M116.760090
doi: 10.1074/jbc.M116.760090
pubmed: 27899449
Hua R, Cheng D, Coyaud E, Freeman S, Di Pietro E, Wang Y, Vissa A, Yip CM, Fairn GD, Braverman N, Brumell JH, Trimble WS, Raught B, Kim PK (2017) VAPs and ACBD5 tether peroxisomes to the ER for peroxisome maintenance and lipid homeostasis. J Cell Biol 216:367–377. https://doi.org/10.1083/jcb.201608128
doi: 10.1083/jcb.201608128
pubmed: 28108526
pmcid: 5294787
Nazarko TY, Ozeki K, Till A, Ramakrishnan G, Lotfi P, Yan M, Subramani S (2014) Peroxisomal Atg37 binds Atg30 or palmitoyl-CoA to regulate phagophore formation during pexophagy. J Cell Biol 204:541–557. https://doi.org/10.1083/jcb.201307050
doi: 10.1083/jcb.201307050
pubmed: 24535825
pmcid: 3926955
Ferdinandusse S, Falkenberg KD, Koster J, Mooyer PA, Jones R, van Roermund CWT, Pizzino A, Schrader M, Wanders RJA, Vanderver A, Waterham HR (2017) ACBD5 deficiency causes a defect in peroxisomal very long-chain fatty acid metabolism. J Med Genet 54:330–337. https://doi.org/10.1136/jmedgenet-2016-104132
doi: 10.1136/jmedgenet-2016-104132
pubmed: 27799409
Dirkx R, Meyhi E, Asselberghs S, Reddy J, Baes M, Van Veldhoven PP (2007) Beta-oxidation in hepatocyte cultures from mice with peroxisomal gene knockouts. Biochem Biophys Res Commun 357:718–723. https://doi.org/10.1016/j.bbrc.2007.03.198
doi: 10.1016/j.bbrc.2007.03.198
pubmed: 17442273
Abe S, Nagai T, Masukawa M, Okumoto K, Homma Y, Fujiki Y, Mizuno K (2017) Localization of protein kinase NDR2 to peroxisomes and its role in ciliogenesis. J Biol Chem 292:4089–4098. https://doi.org/10.1074/jbc.M117.775916
doi: 10.1074/jbc.M117.775916
pubmed: 28122914
pmcid: 5354478
Handa JT (2012) How does the macula protect itself from oxidative stress? Mol Aspects Med 33:418–435. https://doi.org/10.1016/j.mam.2012.03.006
doi: 10.1016/j.mam.2012.03.006
pubmed: 22503691
pmcid: 3392444
Dieuaide-Noubhani M, Novikov D, Vandekerckhove J, Veldhoven PP, Mannaerts GP (1997) Identification and characterization of the 2-enoyl-CoA hydratases involved in peroxisomal beta-oxidation in rat liver. Biochem J 321(Pt 1):253–259
doi: 10.1042/bj3210253
pubmed: 9003427
pmcid: 1218062
Bazan NG (2009) Cellular and molecular events mediated by docosahexaenoic acid-derived neuroprotectin D1 signaling in photoreceptor cell survival and brain protection. Prostaglandins Leukot Essent Fatty Acids 81:205–211. https://doi.org/10.1016/j.plefa.2009.05.024
doi: 10.1016/j.plefa.2009.05.024
pubmed: 19520558
pmcid: 2756692
Abu-Safieh L, Alrashed M, Anazi S, Alkuraya H, Khan AO, Al-Owain M, Al-Zahrani J, Al-Abdi L, Hashem M, Al-Tarimi S, Sebai MA, Shamia A, Ray-Zack MD, Nassan M, Al-Hassnan ZN, Rahbeeni Z, Waheeb S, Alkharashi A, Abboud E, Al-Hazzaa SA, Alkuraya FS (2013) Autozygome-guided exome sequencing in retinal dystrophy patients reveals pathogenetic mutations and novel candidate disease genes. Genome Res 23:236–247. https://doi.org/10.1101/gr.144105.112
doi: 10.1101/gr.144105.112
pubmed: 23105016
pmcid: 3561865
Ferdinandusse S, Denis S, van Roermund CWT, Preece MA, Koster J, Ebberink MS, Waterham HR, Wanders RJA (2018) A novel case of ACOX2 deficiency leads to recognition of a third human peroxisomal acyl-CoA oxidase. Biochim Biophys Acta 1864:952–958. https://doi.org/10.1016/j.bbadis.2017.12.032
doi: 10.1016/j.bbadis.2017.12.032
Gorgas K, Teigler A, Komljenovic D, Just WW (2006) The ether lipid-deficient mouse: tracking down plasmalogen functions. Biochim Biophys Acta 1763:1511–1526. https://doi.org/10.1016/j.bbamcr.2006.08.038
doi: 10.1016/j.bbamcr.2006.08.038
pubmed: 17027098
Rodemer C, Thai TP, Brugger B, Kaercher T, Werner H, Nave KA, Wieland F, Gorgas K, Just WW (2003) Inactivation of ether lipid biosynthesis causes male infertility, defects in eye development and optic nerve hypoplasia in mice. Hum Mol Genet 12:1881–1895
doi: 10.1093/hmg/ddg191
pubmed: 12874108